Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle

Ewen F. Kirkness; Brian J. Haas; Weilin Sun; Henk R. Braig; M. Alejandra Perotti; John M. Clark; Si Hyeock Lee; Hugh M. Robertson; Ryan C. Kennedy; Eran Elhaik; Daniel Gerlach; Evgenia V. Kriventseva; Christine G. Elsik; Dan Graur; Catherine A. Hill; Jan A. Veenstra; Brian Walenz; José Manuel C. Tubío; José M. C. Ribeiro; Julio Rozas; J. Spencer Johnston; Justin T. Reese; Aleksandar Popadic; Marta Tojo; Didier Raoult; David L. Reed; Yoshinori Tomoyasu; Emily Krause; Omprakash Mittapalli; Venu M. Margam; Hong-Mei Li; Jason M. Meyer; Reed M. Johnson; Jeanne Romero-Severson; Janice Pagel VanZee; David Alvarez-Ponce; Filipe G. Vieira; Montserrat Aguadé; Sara Guirao-Rico; Juan M. Anzola; Kyong S. Yoon; Joseph P. Strycharz; Maria F. Unger; Scott Christley; Neil F. Lobo; Manfredo J. Seufferheld; NaiKuan Wang; Gregory A. Dasch; Claudio J. Struchiner; Greg Madey; Linda I. Hannick; Shelby Bidwell; Vinita Joardar; Elisabet Caler; Renfu Shao; Stephen C. Barker; Stephen Cameron; Robert V. Bruggner; Allison Regier; Justin Johnson; Lakshmi Viswanathan; Terry R. Utterback; Granger G. Sutton; Daniel Lawson; Robert M. Waterhouse; J. Craig Venter; Robert L. Strausberg; May R. Berenbaum; Frank H. Collins; Evgeny M. Zdobnov; Barry R. Pittendrigh

doi:10.1073/pnas.1003379107

Contributed by May R. Berenbaum, April 14, 2010 (sent for review February 10, 2010)
↵ ¹E.F.K., E.M.Z., and B.R.P. contributed equally to this work.

Abstract

As an obligatory parasite of humans, the body louse (Pediculus humanus humanus) is an important vector for human diseases, including epidemic typhus, relapsing fever, and trench fever. Here, we present genome sequences of the body louse and its primary bacterial endosymbiont Candidatus Riesia pediculicola. The body louse has the smallest known insect genome, spanning 108 Mb. Despite its status as an obligate parasite, it retains a remarkably complete basal insect repertoire of 10,773 protein-coding genes and 57 microRNAs. Representing hemimetabolous insects, the genome of the body louse thus provides a reference for studies of holometabolous insects. Compared with other insect genomes, the body louse genome contains significantly fewer genes associated with environmental sensing and response, including odorant and gustatory receptors and detoxifying enzymes. The unique architecture of the 18 minicircular mitochondrial chromosomes of the body louse may be linked to the loss of the gene encoding the mitochondrial single-stranded DNA binding protein. The genome of the obligatory louse endosymbiont Candidatus Riesia pediculicola encodes less than 600 genes on a short, linear chromosome and a circular plasmid. The plasmid harbors a unique arrangement of genes required for the synthesis of pantothenate, an essential vitamin deficient in the louse diet. The human body louse, its primary endosymbiont, and the bacterial pathogens that it vectors all possess genomes reduced in size compared with their free-living close relatives. Thus, the body louse genome project offers unique information and tools to use in advancing understanding of coevolution among vectors, symbionts, and pathogens.

Footnotes

⁵To whom correspondence should be addressed. E-mail: pittendr{at}illinois.edu.
Author contributions: E.F.K., B.J.H., J.M.C., H.M.R., R.C.K., E.E., C.G.E., D. Graur, C.A.H., B.W., J.M.C.T., J.M.C.R., J.R., J.S.J., J.T.R., M.T., D.L.R., O.M., V.M.M., J.M.M., J.R.-S., J.P.V., M.A., J.M.A., K.S.Y., J.P.S., M.F.U., S. Christley, N.F.L., G.A.D., C.J.S., G.M., S. Cameron, A.R., G.G.S., J.C.V., R.L.S., F.H.C., E.M.Z., and B.R.P. designed research; B.J.H., W.S., J.M.C., S.H.L., R.C.K., E.E., D. Gerlach, E.V.K., C.G.E., D. Graur, C.A.H., J.A.V., B.W., J.M.C.R., J.R., J.S.J., J.T.R., A.P., Y.T., M.T., D.R., D.L.R., E.K., O.M., H.-M.L., J.M.M., R.J., J.R.-S., J.P.V., D.A.-P., F.G.V., M.A., S.G.-R., J.M.A., K.S.Y., J.P.S., M.F.U., S. Christley, M.J.S., N.W., C.J.S., R.S., S.C.B., A.R., J.J., L.V., T.R.U., D.L., R.M.W., M.R.B., E.M.Z., and B.R.P. performed research; J.M.C., R.C.K., E.E., C.G.E., D. Graur, C.A.H., J.M.C.T., J.S.J., J.T.R., M.T., J.M.M., J.R.-S., J.M.A., K.S.Y., J.P.S., M.F.U., S. Christley, L.I.H., V.J., E.C., R.S., S.C.B., R.V.B., L.V., R.M.W., and E.M.Z., contributed new reagents or analytic tools; E.F.K., W.S., H.R.B., M.A.P., S.H.L., H.M.R., R.C.K., D. Gerlach, E.V.K., J.A.V., B.W., J.M.C.T., J.M.C.R., J.R., A.P., Y.T., M.T., D.L.R., H.-M.L., R.J., J.R.-S., D.A.-P., F.G.V., M.A., S.G.-R., K.S.Y., J.P.S., M.F.U., S. Christley, M.J.S., N.W., G.A.D., C.J.S., L.I.H., S.C.B., V.J., E.C., R.S., S. Cameron, R.V.B., A.R., J.J., D.L., R.M.W., M.R.B., F.H.C., E.M.Z., and B.R.P. analyzed data; and E.F.K., B.J.H., W.S., H.R.B., M.A.P., S.H.L., H.M.R., R.C.K., B.W., J.M.C.T., J.R., A.P., Y.T., M.T., D.R., D.L.R., O.M., R.J., D.A.-P., F.G.V., M.A., S.G.-R., J.M.A., K.S.Y., J.P.S., M.F.U., S. Christley, G.M., S. Cameron, A.R., R.M.W., M.R.B., F.H.C., E.M.Z., and B.R.P. wrote the paper.
The authors declare no conflict of interest.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AAZO00000000, NC_014109, and NC_013962).
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